Abstract
There is a general lack of understanding about how communities of bacteria respond to exogenous toxins such as antibiotics. Most of our understanding of community-level stress responses comes from the study of stationary biofilm communities. Although several community behaviors and production of specific biomolecules affecting biofilm development and associated behavior have been described for Pseudomonas aeruginosa and other bacteria, we have little appreciation for the production and dispersal of secreted metabolites within the 2D and 3D spaces they occupy as they colonize, spread, and grow on surfaces. Here we specifically studied the phenotypic responses and spatial variability of alkyl quinolones, including the Pseudomonas quinolone signal (PQS) and members of the alkyl hydroxyquinoline (AQNO) subclass, in P. aeruginosa plate-assay swarming communities. We found that PQS production was not a universal signaling response to antibiotics, as tobramycin elicited an alkyl quinolone response, whereas carbenicillin did not. We also found that PQS and AQNO profiles in response to tobramycin were markedly distinct and influenced these swarms on different spatial scales. At some tobramycin exposures, P. aeruginosa swarms produced alkyl quinolones in the range of 150 μm PQS and 400 μm AQNO that accumulated as aggregates. Our collective findings show that the distribution of alkyl quinolones can vary by several orders of magnitude within the same swarming community. More notably, our results suggest that multiple intercellular signals acting on different spatial scales can be triggered by one common cue.
Highlights
There is a general lack of understanding about how communities of bacteria respond to exogenous toxins such as antibiotics
We show that the production of alkyl quinolones (AQs)4 by P. aeruginosa swarming communities is substantial, and quinolone secretion varies drastically when exposed to the aminoglycoside antibiotic tobramycin as opposed to the -lactam antibiotic carbenicillin
In the absence of antibiotics, our in situ observations of P. aeruginosa swarms revealed that the Pseudomonas quinolone signal (PQS) and alkyl hydroxyquinoline (AQNO) subclasses act on different spatial scales within plate-assay prebiofilm swarm communities
Summary
There is a general lack of understanding about how communities of bacteria respond to exogenous toxins such as antibiotics. We studied the phenotypic responses and spatial variability of alkyl quinolones, including the Pseudomonas quinolone signal (PQS) and members of the alkyl hydroxyquinoline (AQNO) subclass, in P. aeruginosa plate-assay swarming communities. PQS response to antibiotics in P. aeruginosa swarms lar cyclic-di-GMP levels are low, extracellular polymeric substance production is down-regulated, and cells are actively growing, resulting in the hypothesis that antimicrobial survival in swarming communities is associated with high cell density [3, 13, 14]. The AQs belonging to the PQS pathway participate in processes as diverse as intercellular quorum-sensing signaling, virulence regulation, biofilm development, iron chelation, antimicrobial activity, stress response, and control of cell death (15, 18 –27). In the absence of antibiotics, our in situ observations of P. aeruginosa swarms revealed that the PQS and AQNO subclasses act on different spatial scales within plate-assay prebiofilm swarm communities. Surprising findings open a new window into P. aeruginosa community behavior, which promises to provide deep insights into the spatial signaling and motile-to-sessile transition
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